Downregulation of microRNA-1 in esophageal squamous cell carcinoma correlates with an advanced clinical stage and its overexpression inhibits cell migration and invasion

Yao,Li; Zhang,Yi; Zhu,Qiao; Li,Xinyi; Zhu,Shaojun; Gong,Li; Han,Xiujuan; Lan,Miao; Li,Shanqu; Zhang,Wei; Li,Yanhong

doi:10.3892/ijmm.2015.2094

Downregulation of microRNA-1 in esophageal squamous cell carcinoma correlates with an advanced clinical stage and its overexpression inhibits cell migration and invasion

Authors:
- Li Yao
- Yi Zhang
- Qiao Zhu
- Xinyi Li
- Shaojun Zhu
- Li Gong
- Xiujuan Han
- Miao Lan
- Shanqu Li
- Wei Zhang
- Yanhong Li
View Affiliations

Affiliations: Department of Pathology, Tangdu Hospital, The Fourth Military Medical University, Xi'an, Shaanxi 710038, P.R. China, Cell Engineering Research Center, The Fourth Military Medical University, Xi'an, Shaanxi 710032, P.R. China, Outpatient Department, Tangdu Hospital, The Fourth Military Medical University, Xi'an, Shaanxi 710038, P.R. China, Department of Gynecology and Obstetrics, Tangdu Hospital, The Fourth Military Medical University, Xi'an, Shaanxi 710038, P.R. China
Published online on: February 9, 2015 https://doi.org/10.3892/ijmm.2015.2094
Pages: 1033-1041

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Esophageal squamous cell carcinoma (ESCC) is one of most common and fatal forms of cancer worldwide. Recent studies have suggested that an aberrant microRNA (miRNA or miR) expression signature exists in ESCC. In the present study, in order to determine the involvement of miRNA in the development and progression of ESCC, the expression profiles of miRNA in 8 paired ESCC tissues and corresponding normal esophageal tissues were analyzed by miRNA microarray. A total of 43 differentially expressed miRNAs, including 27 downregulated and 16 upregulated miRNAs were found in the ESCC tissue samples. Among these miRNAs, we found that miR-1 was significantly downregulated. Subsequently, the expression of miR-1 was validated in 64 pairs of primary ESCC samples by RT-qPCR. The expression level of miR-1 was found to be frequently decreased, and significantly correlated with tumor invasion and an advanced clinical stage (P=0.022 and P=0.028, respectively). In addition, functional assays revealed that miR-1 inhibited cell proliferation, clonogenicity, cell invasion and migration. Bioinformatics analyses identified the major biological processes that were targeted by miR-1. These results suggest that miR-1 has a tumor-suppressive effect on the development and progression of ESCC. The findings of this study may contribute to the further understanding of the functions of miR-1 in ESCC.

View Figures

View References

1	Mathé EA, Nguyen GH, Bowman ED, et al: MicroRNA expression in squamous cell carcinoma and adenocarcinoma of the esophagus: associations with survival. Clin Cancer Res. 15:6192–6200. 2009. View Article : Google Scholar : PubMed/NCBI
2	Matsushima K, Isomoto H, Kohno S and Nakao K: MicroRNAs and esophageal squamous cell carcinoma. Digestion. 82:138–144. 2010. View Article : Google Scholar : PubMed/NCBI
3	Feber A, Xi L, Pennathur A, et al: MicroRNA prognostic signature for nodal metastases and survival in esophageal adenocarcinoma. Ann Thorac Surg. 91:1523–1530. 2011. View Article : Google Scholar : PubMed/NCBI
4	Su M, Liu M, Tian DP, et al: Temporal trends of esophageal cancer during 1995–2004 in Nanao Island, an extremely high-risk area in China. Eur J Epidemiol. 22:43–48. 2007. View Article : Google Scholar
5	Enzinger PC and Mayer RJ: Esophageal cancer. N Engl J Med. 349:2241–2252. 2003. View Article : Google Scholar : PubMed/NCBI
6	Iorio MV and Croce CM: MicroRNAs in cancer: small molecules with a huge impact. J Clin Oncol. 27:5848–5856. 2009. View Article : Google Scholar : PubMed/NCBI
7	Ng EK, Chong WW, Jin H, et al: Differential expression of microRNAs in plasma of patients with colorectal cancer: a potential marker for colorectal cancer screening. Gut. 58:1375–1381. 2009. View Article : Google Scholar : PubMed/NCBI
8	Hui A, How C, Ito E and Liu FF: Micro-RNAs as diagnostic or prognostic markers in human epithelial malignancies. BMC Cancer. 11:5002011. View Article : Google Scholar : PubMed/NCBI
9	Mori Y, Ishiguro H, Kuwabara Y, et al: MicroRNA-21 induces cell proliferation and invasion in esophageal squamous cell carcinoma. Mol Med Rep. 2:235–239. 2009.PubMed/NCBI
10	Ma WJ, Lv GD, Tuersun A, et al: Role of microRNA-21 and effect on PTEN in Kazakh’s esophageal squamous cell carcinoma. Mol Biol Rep. 38:3253–3260. 2011. View Article : Google Scholar
11	Melar-New M and Laimins LA: Human papillomaviruses modulate expression of microRNA 203 upon epithelial differentiation to control levels of p63 proteins. J Virol. 84:5212–5221. 2010. View Article : Google Scholar : PubMed/NCBI
12	Matsushima K, Isomoto H, Yamaguchi N, et al: miRNA-205 modulates cellular invasion and migration via regulating zinc finger E-box binding homeobox 2 expression in esophageal squamous cell carcinoma cells. J Transl Med. 9:302011. View Article : Google Scholar : PubMed/NCBI
13	Calin GA, Dumitru CD, Shimizu M, et al: Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA. 99:15524–15529. 2002. View Article : Google Scholar : PubMed/NCBI
14	Hamfjord J, Stangeland AM, Hughes T, et al: Differential expression of miRNAs in colorectal cancer: comparison of paired tumor tissue and adjacent normal mucosa using high-throughput sequencing. PLoS One. 7:e341502012. View Article : Google Scholar : PubMed/NCBI
15	Heidersbach A, Saxby C, Carver-Moore K, et al: microRNA-1 regulates sarcomere formation and suppresses smooth muscle gene expression in the mammalian heart. Elife. 2:e013232013. View Article : Google Scholar : PubMed/NCBI
16	Wystub K, Besser J, Bachmann A, Boettger T and Braun T: miR-1/133a clusters cooperatively specify the cardiomyogenic lineage by adjustment of myocardin levels during embryonic heart development. PLoS Genet. 9:e10037932013. View Article : Google Scholar : PubMed/NCBI
17	Townley-Tilson WH, Callis TE and Wang D: MicroRNAs 1, 133, and 206: critical factors of skeletal and cardiac muscle development, function, and disease. Int J Biochem Cell Biol. 42:1252–1255. 2010. View Article : Google Scholar : PubMed/NCBI
18	Tahara H, Kay MA, Yasui W and Tahara E: MicroRNAs in Cancer: the 22nd Hiroshima Cancer Seminar/the 4th Japanese Association for RNA Interference Joint International Symposium, 30 August 2012, Grand Prince Hotel Hiroshima. Jpn J Clin Oncol. 43:579–582. 2013. View Article : Google Scholar : PubMed/NCBI
19	Furukawa S, Kawasaki Y, Miyamoto M, Hiyoshi M, Kitayama J and Akiyama T: The miR-1-NOTCH3-Asef pathway is important for colorectal tumor cell migration. PLoS One. 8:e806092013. View Article : Google Scholar : PubMed/NCBI
20	Yoshino H, Chiyomaru T, Enokida H, et al: The tumour-suppressive function of miR-1 and miR-133a targeting TAGLN2 in bladder cancer. Br J Cancer. 104:808–818. 2011. View Article : Google Scholar : PubMed/NCBI
21	Nohata N, Sone Y, Hanazawa T, et al: miR-1 as a tumor suppressive microRNA targeting TAGLN2 in head and neck squamous cell carcinoma. Oncotarget. 2:29–42. 2011.PubMed/NCBI
22	Wang F, Song G, Liu M, Li X and Tang H: miRNA-1 targets fibronectin1 and suppresses the migration and invasion of the HEp2 laryngeal squamous carcinoma cell line. FEBS Lett. 585:3263–3269. 2011. View Article : Google Scholar : PubMed/NCBI
23	Wu CD, Kuo YS, Wu HC and Lin CT: MicroRNA-1 induces apoptosis by targeting prothymosin alpha in nasopharyngeal carcinoma cells. J Biomed Sci. 18:802011. View Article : Google Scholar : PubMed/NCBI